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Citations to this article

Continuous treatment with IL-15 exhausts human NK cells via a metabolic defect
Martin Felices, … , Bruce R. Blazar, Jeffrey S. Miller
Martin Felices, … , Bruce R. Blazar, Jeffrey S. Miller
Published February 8, 2018
Citation Information: JCI Insight. 2018;3(3):e96219. https://doi.org/10.1172/jci.insight.96219.
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Research Article Immunology Article has an altmetric score of 10

Continuous treatment with IL-15 exhausts human NK cells via a metabolic defect

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Abstract

NK cell–based immunotherapies have been gaining traction in the clinic for treatment of cancer. IL-15 is currently being used in number of clinical trials to improve NK cell expansion and function. The objective of this study is to evaluate the effect of repetitive IL-15 exposure on NK cells. An in vitro model in which human NK cells are continuously (on on on) or intermittently (on off on) treated with IL-15 was used to explore this question. After treatment, cells were evaluated for proliferation, survival, cell cycle gene expression, function, and metabolic processes. Our data indicate that continuous treatment of NK cells with IL-15 resulted in decreased viability and a cell cycle arrest gene expression pattern. This was associated with diminished signaling, decreased function both in vitro and in vivo, and reduced tumor control. NK cells continuously treated with IL-15 also displayed a reduced mitochondrial respiration profile when compared with NK cells treated intermittently with IL-15. This profile was characterized by a decrease in the spare respiratory capacity that was dependent on fatty acid oxidation (FAO). Limiting the strength of IL-15 signaling via utilization of an mTOR inhibitor rescued NK cell functionality in the group continuously treated with IL-15. The findings presented here show that human NK cells continuously treated with IL-15 undergo a process consistent with exhaustion that is accompanied by a reduction in FAO. These findings should inform IL-15–dosing strategies in NK cell cancer immunotherapeutic settings.

Authors

Martin Felices, Alexander J. Lenvik, Ron McElmurry, Sami Chu, Peter Hinderlie, Laura Bendzick, Melissa A. Geller, Jakub Tolar, Bruce R. Blazar, Jeffrey S. Miller

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Insights into the anti-cancer mechanisms of interleukin-15 from engineered cytokine therapies
Jamie Spangler
Journal of Clinical Investigation 2021
Activation of ADAM17 by IL-15 Limits Human NK Cell Proliferation
HK Mishra, KJ Dixon, N Pore, M Felices, JS Miller, B Walcheck
Frontiers in immunology 2021
Metabolic and Mitochondrial Functioning in Chimeric Antigen Receptor (CAR)—T Cells
AH M., JC Halpin, M Mollaei, SW Bell, N Hirankarn, AD McLellan
Cancers 2021
Targeting a cytokine checkpoint enhances the fitness of armored cord blood CAR-NK cells
M Daher, R Basar, E Gokdemir, N Baran, N Uprety, AK Cortes, M Mendt, LN Kerbauy, PP Banerjee, M Shanley, N Imahashi, L Li, FL Lim, M Fathi, A Rezvan, V Mohanty, Y Shen, H Shaim, J Lu, G Ozcan, E Ensley, M Kaplan, V Nandivada, M Bdiwi, S Acharya, , X Wan, D Mak, E Liu, XR Jiang, S Ang, L Muniz-Feliciano, Y Li, J Wang, S Kordasti, N Petrov, N Varadarajan, D Marin, L Brunetti, RJ Skinner, S Lyu, L Silva, R Turk, MS Schubert, GR Rettig, MS McNeill, G Kurgan, MA Behlke, H Li, NW Fowlkes, K Chen, M Konopleva, RE Champlin, EJ Shpall, K Rezvani
Blood 2021
Epitranscriptomic Approach: To Improve the Efficacy of ICB Therapy by Co-Targeting Intracellular Checkpoint CISH
S Kumar, P Sarthi, I Mani, MU Ashraf, MH Kang, V Kumar, YS Bae
Cells 2021
A robust platform for expansion and genome editing of primary human natural killer cells
RS Huang, MC Lai, HA Shih, S Lin
Journal of Experimental Medicine 2021
The Effect of Unconventional Cytokine Combinations on NK-Cell Responses to Viral Infection
DE Ochayon, SN Waggoner
Frontiers in immunology 2021
Cytokines Orchestrating the Natural Killer-Myeloid Cell Crosstalk in the Tumor Microenvironment: Implications for Natural Killer Cell-Based Cancer Immunotherapy
S Gaggero, K Witt, M Carlsten, S Mitra
Frontiers in immunology 2021
Chronic IL-15 Stimulation and Impaired mTOR Signaling and Metabolism in Natural Killer Cells During Acute Myeloid Leukemia
B Bou-Tayeh, V Laletin, N Salem, S Just-Landi, J Fares, R Leblanc, M Balzano, YM Kerdiles, G Bidaut, O Hérault, D Olive, M Aurrand-Lions, T Walzer, JA Nunès, C Fauriat
Frontiers in immunology 2021
Revisiting the Role of Natural Killer Cells in Non-Alcoholic Fatty Liver Disease
ML Martínez-Chantar, TC Delgado, N Beraza
Frontiers in immunology 2021
Optimising NK cell metabolism to increase the efficacy of cancer immunotherapy
C Choi, DK Finlay
Stem Cell Research & Therapy 2021
An Alternative Cell Therapy for Cancers: Induced Pluripotent Stem Cell (iPSC)-Derived Natural Killer Cells
LJ Hsu, CL Liu, ML Kuo, CN Shen, CR Shen
Biomedicines 2021
CAR-NK Cells in the Treatment of Solid Tumors
E Wrona, M Borowiec, P Potemski
International journal of molecular sciences 2021
AI-guided discovery of the invariant host response to viral pandemics
D Sahoo, GD Katkar, S Khandelwal, M Behroozikhah, A Claire, V Castillo, C Tindle, MK Fuller, S Taheri, TF Rogers, N Beutler, SI Ramirez, SA Rawlings, V Pretorius, DM Smith, DR Burton, LE Alexander, J Duran, S Crotty, JM Dan, S Das, P Ghosh
EBioMedicine 2021
Selection, Expansion, and Unique Pretreatment of Allogeneic Human Natural Killer Cells with Anti-CD38 Monoclonal Antibody for Efficient Multiple Myeloma Treatment
B Motais, S Charvátová, Z Walek, M Hrdinka, R Smolarczyk, T Cichoń, J Czapla, S Giebel, M Šimíček, T Jelínek, T Ševčíková, J Sobotka, Z Kořístek, R Hájek, JR Bagó
Cells 2021
Enhancing a Natural Killer: Modification of NK Cells for Cancer Immunotherapy
R Islam, A Pupovac, V Evtimov, N Boyd, R Shu, R Boyd, A Trounson
Cells 2021
iPSC-Derived Natural Killer Cells for Cancer Immunotherapy
P Karagiannis, SI Kim
Molecules and Cells 2021
Short-course IL-15 given as a continuous infusion led to a massive expansion of effective NK cells: implications for combination therapy with antitumor antibodies
SP Dubois, MD Miljkovic, TA Fleisher, S Pittaluga, J Hsu-Albert, BR Bryant, MN Petrus, LP Perera, JR Müller, JH Shih, TA Waldmann, KC Conlon
Journal for ImmunoTherapy of Cancer 2021
Time-resolved systems immunology reveals a late juncture linked to fatal COVID-19
C Liu, AJ Martins, WW Lau, N Rachmaninoff, J Chen, L Imberti, D Mostaghimi, DL Fink, PD Burbelo, K Dobbs, OM Delmonte, N Bansal, L Failla, A Sottini, E Quiros-Roldan, KL Han, BA Sellers, F Cheung, R Sparks, TW Chun, S Moir, MS Lionakis, C Rossi, HC Su, DB Kuhns, JI Cohen, LD Notarangelo, JS Tsang, MS Abers, R Apps, M Bosticardo, P Milanez-Almeida, MP Mulè, E Shaw, Y Zhang, F Castelli, ML Muiesan, G Tomasoni, F Scolari, A Tucci
Cell 2021
Interleukin-15 in Outcomes of Pregnancy
SM Gordon
International journal of molecular sciences 2021
PRDX-1 Supports the Survival and Antitumor Activity of Primary and CAR-Modified NK Cells under Oxidative Stress
Klopotowska M, Bajor M, Graczyk-Jarzynka A, Kraft A, Pilch Z, Zhylko A, Firczuk M, Baranowska I, Lazniewski M, Plewczynski D, Goral A, Soroczynska K, Domagala J, Marhelava K, Slusarczyk A, Retecki K, Ramji K, Krawczyk M, Temples MN, Sharma B, Lachota M, Netskar H, Malmberg KJ, Zagozdzon R, Winiarska M
Cancer immunology research 2021
Minimal PD-1 expression in mouse and human NK cells under diverse conditions
Sean J. Judge, Cordelia Dunai, Ethan G. Aguilar, Sarah C. Vick, Ian R. Sturgill, Lam T. Khuat, Kevin M. Stoffel, Jonathan Van Dyke, Dan L. Longo, Morgan A. Darrow, Stephen K. Anderson, Bruce R. Blazar, Arta M. Monjazeb, Jonathan S. Serody, Robert J. Canter, William J. Murphy
Journal of Clinical Investigation 2020
"Inflammescent" CX3CR1+CD57+ CD8 T-cells are generated and expanded by IL-15
Stephen R. Morris, Bonnie Chen, Joseph C. Mudd, Soumya Panigrahi, Carey L. Shive, Scott F. Sieg, Cheryl M. Cameron, David A. Zidar, Nicholas T. Funderburg, Souheil-Antoine Younes, Benigno Rodriguez, Sara Gianella, Michael M. Lederman, Michael L. Freeman
JCI Insight 2020
Age-severity matched cytokine profiling reveals specific signatures in Covid-19 patients
R Angioni, R Sánchez-Rodríguez, F Munari, N Bertoldi, D Arcidiacono, S Cavinato, D Marturano, A Zaramella, S Realdon, A Cattelan, A Viola, B Molon
Cell Death and Disease 2020
Metabolic Reprograming via Deletion of CISH in Human iPSC-Derived NK Cells Promotes In Vivo Persistence and Enhances Anti-tumor Activity
H Zhu, RH Blum, D Bernareggi, EH Ask, Z Wu, HJ Hoel, Z Meng, C Wu, KL Guan, KJ Malmberg, DS Kaufman
Cell Stem Cell 2020
IL15 Stimulation with TIGIT Blockade Reverses CD155-mediated NK-Cell Dysfunction in Melanoma
JM Chauvin, M Ka, O Pagliano, C Menna, Q Ding, R DeBlasio, C Sanders, J Hou, XY Li, S Ferrone, D Davar, JM Kirkwood, RJ Johnston, AJ Korman, MJ Smyth, HM Zarour
Clinical cancer research 2020
Analysis of Human Natural Killer Cell Metabolism
J Traba, TA Waldmann, OM Anton
Journal of visualized experiments : JoVE 2020
NK cells for cancer immunotherapy
N Shimasaki, A Jain, D Campana
Nature Reviews Drug Discovery 2020
Interleukin-15 and cancer: some solved and many unsolved questions
PF Fiore, SD Matteo, N Tumino, FR Mariotti, G Pietra, S Ottonello, S Negrini, B Bottazzi, L Moretta, E Mortier, B Azzarone
Journal for ImmunoTherapy of Cancer 2020
Inducible MyD88/CD40 synergizes with IL-15 to enhance antitumor efficacy of CAR-NK cells
X Wang, DL Jasinski, JL Medina, DM Spencer, AE Foster, JH Bayle
Blood Advances 2020
Deciphering Natural Killer Cell Homeostasis
A Pfefferle, B Jacobs, A Haroun-Izquierdo, L Kveberg, E Sohlberg, KJ Malmberg
Frontiers in immunology 2020
Metabolism of Natural Killer Cells and Other Innate Lymphoid Cells
J Cong
Frontiers in immunology 2020
Characterizing the Dysfunctional NK Cell: Assessing the Clinical Relevance of Exhaustion, Anergy, and Senescence
SJ Judge, WJ Murphy, RJ Canter
Frontiers in Cellular and Infection Microbiology 2020
Immunomodulatory Effects of IL-2 and IL-15; Implications for Cancer Immunotherapy
Y Yang, A Lundqvist
Cancers 2020
Natural Killer Cells in Immunotherapy: Are We Nearly There?
M Bachiller, AM Battram, L Perez-Amill, B Martín-Antonio
Cancers 2020
Recalling the Biological Significance of Immune Checkpoints on NK Cells: A Chance to Overcome LAG3, PD1, and CTLA4 Inhibitory Pathways by Adoptive NK Cell Transfer?
PM Lanuza, C Pesini, MA Arias, C Calvo, A Ramirez-Labrada, J Pardo
Frontiers in immunology 2020
Indirect Impact of PD-1/PD-L1 Blockade on a Murine Model of NK Cell Exhaustion
M Alvarez, F Simonetta, J Baker, AR Morrison, AS Wenokur, A Pierini, P Berraondo, RS Negrin
Frontiers in immunology 2020
Innate Cytokine Induced Early Release of IFNγ and CC Chemokines from Hypoxic Human NK Cells Is Independent of Glucose
SY Velásquez, BS Himmelhan, N Kassner, A Coulibaly, J Schulte, K Brohm, HA Lindner
Cells 2020
IL-15 in the Combination Immunotherapy of Cancer
TA Waldmann, S Dubois, MD Miljkovic, KC Conlon
Frontiers in immunology 2020
NK-Cell-Mediated Targeting of Various Solid Tumors Using a B7-H3 Tri-Specific Killer Engager In Vitro and In Vivo
DA Vallera, S Ferrone, B Kodal, P Hinderlie, L Bendzick, B Ettestad, C Hallstrom, NA Zorko, A Rao, N Fujioka, CJ Ryan, MA Geller, JS Miller, M Felices
Cancers 2020
Use of CAR-Transduced Natural Killer Cells in CD19-Positive Lymphoid Tumors
E Liu, D Marin, P Banerjee, HA Macapinlac, P Thompson, R Basar, LN Kerbauy, B Overman, P Thall, M Kaplan, V Nandivada, I Kaur, AN Cortes, K Cao, M Daher, C Hosing, EN Cohen, P Kebriaei, R Mehta, S Neelapu, Y Nieto, M Wang, W Wierda, M Keating, R Champlin, EJ Shpall, K Rezvani
New England Journal of Medicine 2020
Directed Differentiation of Mobilized Hematopoietic Stem and Progenitor Cells into Functional NK Cells with Enhanced Antitumor Activity
P Oberoi, K Kamenjarin, JF Ossa, B Uherek, H Bönig, WS Wels
Cells 2020
Regulation of murine NK cell exhaustion through the activation of the DNA damage repair pathway
Maite Alvarez, Federico Simonetta, Jeanette Baker, Antonio Pierrini, Arielle S Wenokur, Alyssa R Morrison, William Murphy, Robert Negrin
JCI Insight 2019
Interleukin-15 (dys)regulation of lymphoid homeostasis: Implications for therapy of autoimmunity and cancer
TA Waldmann, MD Miljkovic, KC Conlon
Journal of Experimental Medicine 2019
Adipocytes: A Novel Target for IL-15/IL-15Rα Cancer Gene Therapy
R Xiao, AG Mansour, W Huang, LA Chrislip, RK Wilkins, NJ Queen, Y Youssef, HC Mao, MA Caligiuri, L Cao
Molecular Therapy 2019
NK Cell Hyporesponsiveness: More Is Not Always Better
M Frutoso, E Mortier
International journal of molecular sciences 2019
Genetic reprogramming for NK cell cancer immunotherapy with CRISPR/Cas9
LO Afolabi, AO Adeshakin, MM Sani, J Bi, X Wan
Immunology 2019
The Synergistic Use of IL-15 and IL-21 for the Generation of NK Cells From CD3/CD19-Depleted Grafts Improves Their ex vivo Expansion and Cytotoxic Potential Against Neuroblastoma: Perspective for Optimized Immunotherapy Post Haploidentical Stem Cell Transplantation
A Heinze, B Grebe, M Bremm, S Huenecke, TA Munir, L Graafen, JT Frueh, M Merker, E Rettinger, J Soerensen, T Klingebiel, P Bader, E Ullrich, C Cappel
Frontiers in immunology 2019
Immune Reconstitution Disorders: Spotlight on Interferons
IV Louis
2019
Inducing Fat to Feed a Natural Killer of Malignancy
B Rambaldi, R Romee
Molecular Therapy 2019
Strategies to Augment Natural Killer (NK) Cell Activity against Solid Tumors
Z Chen, Y Yang, LL Liu, A Lundqvist
Cancers 2019
NK Cell Metabolism and Tumor Microenvironment
I Terrén, A Orrantia, J Vitallé, O Zenarruzabeitia, F Borrego
Frontiers in immunology 2019
Harnessing Natural Killer Cell Antitumor Immunity: From the Bench to Bedside
KV Woan, JS Miller
Cancer immunology research 2019
NK Cells for PD-1/PD-L1 blockade immunotherapy- Pinning Down the NK cell
Cordelia Dunai, William Murphy
Journal of Clinical Investigation 2018
Tumor Microenvironment-Induced Immunometabolic Reprogramming of Natural Killer Cells
AM Chambers, KB Lupo, S Matosevic
Frontiers in immunology 2018
Natural killer cells as a therapeutic tool for infectious diseases - current status and future perspectives
S Schmidt, L Tramsen, B Rais, E Ullrich, T Lehrnbecher
Oncotarget 2018
IL-15 regulates fibrosis and inflammation in a mouse model of chronic pancreatitis
M Manohar, HK Kandikattu, AK Verma, A Mishra
AJP Gastrointestinal and Liver Physiology 2018
Highly cytotoxic natural killer cells are associated with poor prognosis in patients with cutaneous T-cell lymphoma
B Mundy-Bosse, N Denlinger, E McLaughlin, N Chakravarti, S Hwang, L Chen, HC Mao, D Kline, Y Youssef, R Kohnken, DA Lee, G Lozanski, AG Freud, P Porcu, B William, MA Caligiuri, A Mishra
Blood Advances 2018

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